The effects of Nembutal on the intracerebellar EEG activity revealed by spectral and fractal analysis

Authors

  • Gordana Stojadinović Department of Neurophysiology, Institute for Biological Research “Siniša Stanković”, National Institute of the Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0001-7155-165X
  • Ljiljana Martać Department of Neurophysiology, Institute for Biological Research “Siniša Stanković”, National Institute of the Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-9931-7328
  • Jelena Podgorac Department of Neurophysiology, Institute for Biological Research “Siniša Stanković”, National Institute of the Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0003-0393-5023
  • Slađana Z. Spasić Department of Life Sciences, Institute for Multidisciplinary Research, University of Belgrade, Kneza Višeslava 1, 11030 Belgrade http://orcid.org/0000-0003-1098-371X
  • Branka Petković Department of Neurophysiology, Institute for Biological Research “Siniša Stanković”, National Institute of the Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0001-7817-4092
  • Slobodan Sekulić Department of Neurology, Faculty of Medicine, University of Novi Sad, Hajduk Veljkova 3, 21000 Novi Sad http://orcid.org/0000-0001-7889-310X
  • Srđan Kesić Department of Neurophysiology, Institute for Biological Research “Siniša Stanković”, National Institute of the Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-2323-9669

Keywords:

Nembutal, intracerebellar EEG, spectral analysis, fractal analysis

Abstract

Paper description:

  • Studies of the effects of anesthetics on functional brain networks are essential to understand changes in brain bioelectrical activity in health and disease.
  • Using spectral and fractal analysis, we recorded the electroencephalographic (EEG) activity at different layers of the cerebellum during nembutal anesthesia.
  • Nembutal induced an increase in delta (0.1-4.0 Hz) and a decrease in theta (4.1-8.0 Hz) EEG frequency ranges, and an increase in the value of Higuchi’s fractal dimension in the cerebellar layers.
  • This study indicates that spectral and fractal analysis can be used complementarily for measuring anesthesia-induced intra-cerebellar EEG dynamics.


Abstract: A detailed analysis of the anesthetic-induced modulation of intracerebellar electrical activity is an important step to understand the functional brain responses to anesthesia. We examined the electrical activity recorded from different cortical layers: molecular layer (ML), Purkinje cell layer (PCL), granular layer (GL) and the white matter (WM) in the vermian part of rat cerebellar lobule V during Nembutal anesthesia using spectral and fractal analysis. Spectral analysis revealed a difference in the mean relative power of delta (0.1-4.0 Hz) and theta (4.1-8.0 Hz) frequencies through the cerebellar layers. Compared to the ML, delta activity increased significantly in the GL, while theta activity decreased in the GL and the WM. Fractal analysis revealed that the mean value of Higuchi’s fractal dimension (HFD) increased, starting from the ML to the WM. Theta activity exhibited a negative correlation with the HFD value in the ML. In contrast, the gamma activity showed a positive correlation with the HFD value in the ML and the GL. The combined use of spectral and fractal analyses revealed that Nembutal displays different effects on rat cerebellar electrical activity, which largely depends on the neurochemical and electrophysiological organization of the cerebellar layers.

https://doi.org/10.2298/ABS200524036S

Received: May 24, 2020; Revised: July 3, 2020; Accepted: August 6, 2020; Published online: August 27, 2020

How to cite this article: Stojadinović G, Martać L, Podgorac J, Spasić SZ, Petković B, Sekulić S, Kesić S. The effects of Nembutal on the intracerebellar EEG activity revealed by spectral and fractal analysis. Arch Biol Sci. 2020;72(3):425-32.

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References

Ching S, Purdon PL, Vijayan S, Kopell NJ, Brown EN. A neurophysiological-metabolic model for burst suppression. Proc Natl Acad Sci U S A. 2012;109(8):3095-100.

Shepherd J, Jones J, Frampton G, Bryant J, Baxter L, Cooper K. Clinical effectiveness and cost-effectiveness of depth of anaesthesia monitoring (E-Entropy, Bispectral Index and Narcotrend): a systematic review and economic evaluation. Health Technol Assess. 2013;17(34):1-264.

Zhang XS, Roy RJ, Jensen EW. EEG complexity as a measure of depth of anesthesia for patients. IEEE transactions on bio-medical engineering. 2001;48(12):1424-33.

Ferenets R, Vanluchene A, Lipping T, Heyse B, Struys MM. Behavior of entropy/complexity measures of the electroencephalogram during propofol-induced sedation: dose-dependent effects of remifentanil. Anesthesiology. 2007;106(4):696-706.

Kekovic G, Stojadinovic G, Martac L, Podgorac J, Sekulic S, Culic M. Spectral and fractal measures of cerebellar and cerebral activity in various types of anesthesia. Acta Neurobiol Exp (Wars). 2010;70(1):67-75.

Spasic S, Kalauzi A, Kesic S, Obradovic M, Saponjic J. Surrogate data modeling the relationship between high frequency amplitudes and Higuchi fractal dimension of EEG signals in anesthetized rats. J Theor Biol. 2011;289:160-6.

Spasic S, Kesic S, Kalauzi A, Saponjic J. Different anesthesia in rat induces distinct inter-structure brain dynamic detected by Higuchi fractal dimension. Fractals. 2011;19(1):113-23.

Kesić S, Spasić SZ. Application of Higuchi’s fractal dimension from basic to clinical neurophysiology: A review. Comput Methods Programs Biomed. 2016;133:55-70.

D’Angelo E. Physiology of the cerebellum. Handb Clin Neurol. 2018;154:85-108.

Sultan F, Glickstein M. The cerebellum: Comparative and animal studies. Cerebellum. 2007;6(3):168-76.

Standring S. Gray’s anatomy: the anatomical basis of clinical practice. 41st ed. Philadelphia: Elsevier Limited; 2016. 1584 p.

Dauth G, Carr D, Gilman S. Cerebellar cortical stimulation effects on EEG activity and seizure after-discharge in anesthetized cats. In: Cooper IS, Riklan M, Snider RS, editors. The cerebellum, epilepsy, and behavior. Boston, MA: Springer; 1974. p. 229-44.

Culic M, Martac Blanusa L, Grbic G, Spasic S, Jankovic B, Kalauzi A. Spectral analysis of cerebellar activity after acute brain injury in anesthetized rats. Acta Neurobiol Exp (Wars). 2005;65(1):11-7.

Rowland NC, Goldberg JA, Jaeger D. Cortico-cerebellar coherence and causal connectivity during slow-wave activity. Neuroscience. 2010;166(2):698-711.

Routtenberg A. Pentobarbital anesthesia of albino rats. J Exp Anal Behav. 1968;11(1):52.

Sanna E, Garau F, Harris RA. Novel properties of homomeric beta 1 gamma-aminobutyric acid type A receptors: actions of the anesthetics propofol and pentobarbital. Mol Pharmacol. 1995;47(2):213-7.

Steinbach JH, Akk G. Modulation of GABA(A) receptor channel gating by pentobarbital. J Physiol. 2001;537(Pt 3):715-33.

Valverde A, Doherty TJ. Anesthesia and analgesia of ruminants. In: Fish RE, Brown MJ, Danneman PJ, Karas AZ, editors. Anesthesia and analgesia in laboratory animals. 2nd ed. London: Academic Press; 2008. p. 385-411.

López-Muñoz F, Ucha-Udabe R, Alamo C. The history of barbiturates a century after their clinical introduction. Neuropsychiatr Dis Treat. 2005;1(4):329-43.

Cooney K. Historical perspective of euthanasia in veterinary medicine. Vet Clin North Am Small Anim Pract. 2020;50(3):489-502.

Tsubokura Y, Kobayashi T, Oshima Y, Hashizume N, Nakai M, Ajimi S, Imatanaka N. Effects of pentobarbital, isoflurane, or medetomidine-midazolam-butorphanol anesthesia on bronchoalveolar lavage fluid and blood chemistry in rats. J Toxicol Sci. 2016;41(5):595-604.

Wu C, Sun D. GABA receptors in brain development, function, and injury. Metab Brain Dis. 2015;30(2):367-79.

Palacios JM, Young WS, 3rd, Kuhar MJ. Autoradiographic localization of gamma-aminobutyric acid (GABA) receptors in the rat cerebellum. Proc Natl Acad Sci U S A. 1980;77(1):670-4.

Fritschy JM, Panzanelli P. Molecular and synaptic organization of GABAA receptors in the cerebellum: Effects of targeted subunit gene deletions. Cerebellum. 2006;5(4):275-85.

Fritschy JM, Panzanelli P, Kralic JE, Vogt KE, Sassoe-Pognetto M. Differential dependence of axo-dendritic and axo-somatic GABAergic synapses on GABAA receptors containing the alpha1 subunit in Purkinje cells. J Neurosci. 2006;26(12):3245-55.

Hirano T. GABA and synaptic transmission in the cerebellum. In: Manto M, Schmahmann JD, Rossi F, Gruol DL, Koibuchi N, editors. Handbook of the cerebellum and cerebellar disorders. Dordrecht: Springer; 2013. p. 881-93.

Hirano T. GABA pathways and receptors. In: Gruol DL, Koibuchi N, Manto M, Molinari M, Schmahmann JD, Shen Y, editors. Essentials of cerebellum and cerebellar disorders. Cham: Springer; 2016. p. 225-9.

Morton SM, Bastian AJ. Relative contributions of balance and voluntary leg-coordination deficits to cerebellar gait ataxia. J Neurophysiol. 2003;89(4):1844-56.

Dressler O, Schneider G, Stockmanns G, Kochs EF. Awareness and the EEG power spectrum: analysis of frequencies. Br J Anaesth. 2004;93(6):806-9.

Spasic S, Kalauzi A, Grbic G, Martac L, Culic M. Fractal analysis of rat brain activity after injury. Med Biol Eng Comput. 2005;43(3):345-8.

Eke A, Herman P, Kocsis L, Kozak LR. Fractal characterization of complexity in temporal physiological signals. Physiol Meas. 2002;23(1):R1-38.

Grbić G, Ćulić M, Martać L, Soković M, Spasić S, Đoković D. Effect of camphor essential oil on rat cerebral cortex activity as manifested by fractal dimension changes. Arch Biol Sci. 2008;60(4):547-53.

Ćulić M, Keković G, Grbić G, Martać L, Soković M, Podgorac J, Sekulić S. Wavelet and fractal analysis of rat brain activity in seizures evoked by camphor essential oil and 1,8-cineole. Gen Physiol Biophys. 2009;28 Spec No:33-40.

Cusenza M, Accardo A, Orsini A. EEG fractal dimension combined with burst suppression ratio as a measure of depth of anesthesia. In: Long M, ed. World Congress on Medical Physics and Biomedical Engineering May 26-31, 2012, Beijing, China. IFMBE Proceedings. 2013;39:497-500. Berlin, Heidelberg: Springer.

Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 5th ed. Cambridge (Massachusetts): Academic Press; 2004. 209 p.

Jovanovic A. Biomedical image and signal processing. School of Mathematics, Un. of Belgrade, E-book. 2004.

Higuchi T. Approach to an irregular time series on the basis of the fractal theory. Physica D: Nonlinear Phenomena. 1988;31(2):277-83.

Klonowski W, Olejarczyk E, Stepienl R, Szelenberger W. New methods of nonlinear and symbolic dynamics in sleep EEG-signal analysis. IFAC Proceedings Volumes. 2003;36(15):241-4.

Ciszewski J, Klonowski W, Stepien R, Jernajczyk W, Karlinski A, Niedzielska K. Application of chaos theory for EEG-signal analysis in patients with seasonal affective disorder. Med Biol Eng Comput. 1999;37(Supplement 1):359-60.

Spasić S, Kalauzi A, Ćulić M, Grbić G, Martać L. Estimation of parameter kmax in fractal analysis of rat brain activity. Ann N Y Acad Sci. 2005;1048:427-9.

’D’Angelo E, Nieus T, Maffei A, Armano S, Rossi P, Taglietti V, Fontana A, Naldi G. Theta-frequency bursting and resonance in cerebellar granule cells: experimental evidence and modeling of a slow k+-dependent mechanism. J Neurosci. 2001;21(3):759-70.

Hartmann MJ, Bower JM. Oscillatory activity in the cerebellar hemispheres of unrestrained rats. J Neurophysiol. 1998;80(3):1598-604.

Radian R, Ottersen OP, Storm-Mathisen J, Castel M, Kanner BI. Immunocytochemical localization of the GABA transporter in rat brain. J Neurosci. 1990;10(4):1319-30.

Morara S, Brecha NC, Marcotti W, Provini L, Rosina A. Neuronal and glial localization of the GABA transporter GAT-1 in the cerebellar cortex. Neuroreport. 1996;7(18):2993-6.

Konopacki J, Golebiewski H, Eckersdorf B, Blaszczyk M, Grabowski R. Theta-like activity in hippocampal formation slices: the effect of strong disinhibition of GABAA and GABAB receptors. Brain Res. 1997;775(1-2):91-8.

Fu Y, Li L, Wang Y, Chu G, Kong X, Wang J. Role of GABAA receptors in EEG activity and spatial recognition memory in aged APP and PS1 double transgenic mice. Neurochem Int. 2019;131:104542.

Middleton SJ, Racca C, Cunningham MO, Traub RD, Monyer H, Knopfel T, Schofield IS, Jenkins A, Whittington MA. High-frequency network oscillations in cerebellar cortex. Neuron. 2008;58(5):763-74.

Klonowski W, Stepien P, Stepien R. Complexity measures of brain electrophysiological activity: In consciousness, under anesthesia, during epileptic seizure, and in physiological sleep. J Psychophysiol. 2010;24(2):131-5.

Zappasodi F, Olejarczyk E, Marzetti L, Assenza G, Pizzella V, Tecchio F. Fractal dimension of EEG activity senses neuronal impairment in acute stroke. PLoS One. 2014;9(6):e100199.

Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489-501.

Koziol LF, Budding D, Andreasen N, D'Arrigo S, Bulgheroni S, Imamizu H, Ito M, Manto M, Marvel C, Parker K, Pezzulo G, Ramnani N, Riva D, Schmahmann J, Vandervert L, Yamazaki T. Consensus paper: the cerebellum's role in movement and cognition. Cerebellum. 2014;13(1):151-77.

Kelly RM, Strick PL. Cerebellar loops with the motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23(23):8432–44.

Negahbani E, Amirfattahi R, Ahmadi B, Dehnavi AM, Rouzbeh M, Zaghari B, Hashemi Z. Electroencephalogram fractal dimension as a measure of depth of anesthesia. In: 3rd International Conference on Information and Communication Technologies: From Theory to Applications (ICTTA); 2018 Ap 7-11; Damascus, Syria. Piscataway, NJ: IEEE; 2008. p. 1-5.

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Published

2020-10-19

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Stojadinović G, Martać L, Podgorac J, Spasić SZ, Petković B, Sekulić S, Kesić S. The effects of Nembutal on the intracerebellar EEG activity revealed by spectral and fractal analysis. Arch Biol Sci [Internet]. 2020Oct.19 [cited 2024Dec.22];72(3):425-32. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/5405

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Vol. 72 No. 3 (2020)

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